1. Cell Biology
  2. Microbiology and Infectious Disease

Stress-activated MAPK signalling controls fission yeast actomyosin ring integrity by modulating formin For3 levels

  1. Elisa Gómez-Gil
  2. Rebeca Martín-García
  3. Jero Vicente-Soler
  4. Alejandro Franco
  5. Beatriz Vázquez-Marín
  6. Francisco Prieto-Ruiz
  7. Teresa Soto
  8. Pilar Pérez
  9. Marisa Madrid  Is a corresponding author
  10. Jose Cansado  Is a corresponding author
  1. Universidad de Murcia, Spain
  2. Instituto de Biología Funcional y Genómica/Universidad de Salamanca, Spain
https://doi.org/10.7554/eLife.57951
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  1. Elisa Gómez-Gil
  2. Rebeca Martín-García
  3. Jero Vicente-Soler
  4. Alejandro Franco
  5. Beatriz Vázquez-Marín
  6. Francisco Prieto-Ruiz
  7. Teresa Soto
  8. Pilar Pérez
  9. Marisa Madrid
  10. Jose Cansado
(2020)
Stress-activated MAPK signalling controls fission yeast actomyosin ring integrity by modulating formin For3 levels
eLife 9:e57951.
https://doi.org/10.7554/eLife.57951
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Abstract

Cytokinesis, which enables the physical separation of daughter cells once mitosis has been completed, is executed in fungal and animal cells by a contractile actin- and myosin-based ring (CAR). In the fission yeast Schizosaccharomyces pombe the formin For3 nucleates actin cables and also co-operates for CAR assembly during cytokinesis. Mitogen-Activated Protein Kinases (MAPKs) regulate essential adaptive responses in eukaryotic organisms to environmental changes. We show that the Stress Activated Protein Kinase pathway (SAPK) and its effector, MAPK Sty1, downregulates CAR assembly in S. pombe when its integrity becomes compromised during cytoskeletal damage and stress by reducing For3 levels. Accurate control of For3 levels by the SAPK pathway may thus represent a novel regulatory mechanism of cytokinesis outcome in response to environmental cues. Conversely, SAPK signalling favours CAR assembly and integrity in its close relative S. japonicus, revealing a remarkable evolutionary divergence of this response within the fission yeast clade.

Data availability

All data generated or analysed during this study are included within the manuscript and supporting files.

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Author details

  1. Elisa Gómez-Gil

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.

  2. Rebeca Martín-García

    Morfogénesis y Polaridad Celular, Instituto de Biología Funcional y Genómica/Universidad de Salamanca, Salamanca, Spain
    Competing interests
    The authors declare that no competing interests exist.

  3. Jero Vicente-Soler

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.

  4. Alejandro Franco

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.

  5. Beatriz Vázquez-Marín

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.

  6. Francisco Prieto-Ruiz

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.

  7. Teresa Soto

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2965-318X

  8. Pilar Pérez

    Morfogénesis y Polaridad Celular, Instituto de Biología Funcional y Genómica/Universidad de Salamanca, Salamanca, Spain
    Competing interests
    The authors declare that no competing interests exist.

  9. Marisa Madrid

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    For correspondence
    marisa@um.es
    Competing interests
    The authors declare that no competing interests exist.

  10. Jose Cansado

    Genetics and Microbiology, Universidad de Murcia, Murcia, Spain
    For correspondence
    jcansado@um.es
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2342-8152

Funding

Ministerio de Economía y Competitividad (BFU2017-82423-P)

  • Jose Cansado

Ministerio de Economía y Competitividad (PGC2018-098924-B-100)

  • Pilar Pérez

Junta de Castilla y Leon (CLU-2017-03)

  • Pilar Pérez

Fundacion Seneca (20856/PI/18)

  • Jose Cansado

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Mohan K Balasubramanian, University of Warwick, United Kingdom

Version history

  1. Received: April 16, 2020
  2. Accepted: September 10, 2020
  3. Accepted Manuscript published: September 11, 2020 (version 1)
  4. Version of Record published: September 23, 2020 (version 2)

Copyright

© 2020, Gómez-Gil et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Elisa Gómez-Gil
  2. Rebeca Martín-García
  3. Jero Vicente-Soler
  4. Alejandro Franco
  5. Beatriz Vázquez-Marín
  6. Francisco Prieto-Ruiz
  7. Teresa Soto
  8. Pilar Pérez
  9. Marisa Madrid
  10. Jose Cansado
(2020)
Stress-activated MAPK signalling controls fission yeast actomyosin ring integrity by modulating formin For3 levels
eLife 9:e57951.
https://doi.org/10.7554/eLife.57951

Share this article

https://doi.org/10.7554/eLife.57951

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Further reading

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    Cytokinesis, the separation of daughter cells at the end of mitosis, relies in animal cells on a contractile actomyosin ring (CAR) composed of actin and class II myosins, whose activity is strongly influenced by regulatory light chain (RLC) phosphorylation. However, in simple eukaryotes such as the fission yeast Schizosaccharomyces pombe, RLC phosphorylation appears dispensable for regulating CAR dynamics. We found that redundant phosphorylation at Ser35 of the S. pombe RLC homolog Rlc1 by the p21-activated kinases Pak1 and Pak2, modulates myosin II Myo2 activity and becomes essential for cytokinesis and cell growth during respiration. Previously, we showed that the stress-activated protein kinase pathway (SAPK) MAPK Sty1 controls fission yeast CAR integrity by downregulating formin For3 levels (Gómez-Gil et al., 2020). Here, we report that the reduced availability of formin For3-nucleated actin filaments for the CAR is the main reason for the required control of myosin II contractile activity by RLC phosphorylation during respiration-induced oxidative stress. Thus, the restoration of For3 levels by antioxidants overrides the control of myosin II function regulated by RLC phosphorylation, allowing cytokinesis and cell proliferation during respiration. Therefore, fine-tuned interplay between myosin II function through Rlc1 phosphorylation and environmentally controlled actin filament availability is critical for a successful cytokinesis in response to a switch to a respiratory carbohydrate metabolism.

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